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On the Origins of Phenotypic Parallelism in Benthic and Limnetic Stickleback

Rapid evolution of similar phenotypes in similar environments, giving rise to in situ parallel adaptation, is an important hallmark of ecological speciation. However, what appears to be in situ adaptation can also arise by dispersal of divergent lineages from elsewhere. We test whether two contrasti...

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Autores principales: Dean, Laura L, Magalhaes, Isabel Santos, D’Agostino, Daniele, Hohenlohe, Paul, MacColl, Andrew D C
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10490448/
https://www.ncbi.nlm.nih.gov/pubmed/37652053
http://dx.doi.org/10.1093/molbev/msad191
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author Dean, Laura L
Magalhaes, Isabel Santos
D’Agostino, Daniele
Hohenlohe, Paul
MacColl, Andrew D C
author_facet Dean, Laura L
Magalhaes, Isabel Santos
D’Agostino, Daniele
Hohenlohe, Paul
MacColl, Andrew D C
author_sort Dean, Laura L
collection PubMed
description Rapid evolution of similar phenotypes in similar environments, giving rise to in situ parallel adaptation, is an important hallmark of ecological speciation. However, what appears to be in situ adaptation can also arise by dispersal of divergent lineages from elsewhere. We test whether two contrasting phenotypes repeatedly evolved in parallel, or have a single origin, in an archetypal example of ecological adaptive radiation: benthic–limnetic three-spined stickleback (Gasterosteus aculeatus) across species pair and solitary lakes in British Columbia. We identify two genomic clusters across freshwater populations, which differ in benthic–limnetic divergent phenotypic traits and separate benthic from limnetic individuals in species pair lakes. Phylogenetic reconstruction and niche evolution modeling both suggest a single evolutionary origin for each of these clusters. We detected strong phylogenetic signal in benthic–limnetic divergent traits, suggesting that they are ancestrally retained. Accounting for ancestral state retention, we identify local adaptation of body armor due to the presence of an intraguild predator, the sculpin (Cottus asper), and environmental effects of lake depth and pH on body size. Taken together, our results imply a predominant role for retention of ancestral characteristics in driving trait distribution, with further selection imposed on some traits by environmental factors.
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spelling pubmed-104904482023-09-09 On the Origins of Phenotypic Parallelism in Benthic and Limnetic Stickleback Dean, Laura L Magalhaes, Isabel Santos D’Agostino, Daniele Hohenlohe, Paul MacColl, Andrew D C Mol Biol Evol Discoveries Rapid evolution of similar phenotypes in similar environments, giving rise to in situ parallel adaptation, is an important hallmark of ecological speciation. However, what appears to be in situ adaptation can also arise by dispersal of divergent lineages from elsewhere. We test whether two contrasting phenotypes repeatedly evolved in parallel, or have a single origin, in an archetypal example of ecological adaptive radiation: benthic–limnetic three-spined stickleback (Gasterosteus aculeatus) across species pair and solitary lakes in British Columbia. We identify two genomic clusters across freshwater populations, which differ in benthic–limnetic divergent phenotypic traits and separate benthic from limnetic individuals in species pair lakes. Phylogenetic reconstruction and niche evolution modeling both suggest a single evolutionary origin for each of these clusters. We detected strong phylogenetic signal in benthic–limnetic divergent traits, suggesting that they are ancestrally retained. Accounting for ancestral state retention, we identify local adaptation of body armor due to the presence of an intraguild predator, the sculpin (Cottus asper), and environmental effects of lake depth and pH on body size. Taken together, our results imply a predominant role for retention of ancestral characteristics in driving trait distribution, with further selection imposed on some traits by environmental factors. Oxford University Press 2023-08-31 /pmc/articles/PMC10490448/ /pubmed/37652053 http://dx.doi.org/10.1093/molbev/msad191 Text en © The Author(s) 2023. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Discoveries
Dean, Laura L
Magalhaes, Isabel Santos
D’Agostino, Daniele
Hohenlohe, Paul
MacColl, Andrew D C
On the Origins of Phenotypic Parallelism in Benthic and Limnetic Stickleback
title On the Origins of Phenotypic Parallelism in Benthic and Limnetic Stickleback
title_full On the Origins of Phenotypic Parallelism in Benthic and Limnetic Stickleback
title_fullStr On the Origins of Phenotypic Parallelism in Benthic and Limnetic Stickleback
title_full_unstemmed On the Origins of Phenotypic Parallelism in Benthic and Limnetic Stickleback
title_short On the Origins of Phenotypic Parallelism in Benthic and Limnetic Stickleback
title_sort on the origins of phenotypic parallelism in benthic and limnetic stickleback
topic Discoveries
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10490448/
https://www.ncbi.nlm.nih.gov/pubmed/37652053
http://dx.doi.org/10.1093/molbev/msad191
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